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Dose-Response Effects of Acute Aerobic Exercise Intensity on Inhibitory Control in Children with Attention Deficit/Hyperactivity

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Dose-Response Effects of Acute Aerobic Exercise Intensity on Inhibitory Control in Children with Attention Deficit/Hyperactivity ORIGINAL RESEARCH published: 18 June 2021 doi: 10.3389/fnhum.2021.617596 Dose-Response Effects of Acute Aerobic Exercise Intensity on Inhibitory Control in Children With Attention Deficit/Hyperactivity Disorder Yu-Jung Tsai 1, Shu-Shih Hsieh 2, Chung-Ju Huang 3 and Tsung-Min Hung 1,4* 1 Department of Physical Education and Sport Sciences, National Taiwan Normal University, Taipei, Taiwan, 2 Department of Psychology, Northeastern University, Boston, MA, United States, 3 Graduate Institute of Sport Pedagogy, University of Taipei, Taipei, Taiwan, 4 Institute for Research Excellence in Learning Science, National Taiwan Normal University, Taipei, Taiwan The present study aimed to examine whether the effect of acute aerobic exercise on inhibitory control of children with attention-deficit/hyperactivity disorder (ADHD) is moderated by exercise intensity. Using a within-subjects design, 25 children with ADHD completed a flanker task with concurrent collection of electroencephalography (EEG) data after three different intensities of treadmill running. The results showed that Edited by: low- and moderate-intensity exercises resulted in shorter reaction times (RTs) relative Sebastian Ludyga, to vigorous-intensity exercise during the incompatible condition of the flanker task University of Basel, Switzerland regardless of task congruency. A P3 congruency effect was observed following low- and Reviewed by: vigorous-intensity exercises but not after moderate-intensity exercise. The mean alpha Aylin Mehren, University of Oldenburg, Germany power, a measure of cortical arousal, increased following low- and moderate-intensity Manuel Mücke, exercises but decreased following vigorous-intensity exercise. In addition, the change in University of Basel, Switzerland arousal level after moderate-intensity exercise was negatively correlated with RT during *Correspondence: Tsung-Min Hung incompatible flanker tasks. The current findings suggest that children with ADHD have [email protected] better inhibitory control following both low- and moderate-intensity exercises relative to vigorous aerobic exercise, which could be characterized by an optimal state of Specialty section: cortical arousal. This article was submitted to Brain Health and Clinical Keywords: intensity, acute exercise, executive function, arousal level, ADHD Neuroscience, a section of the journal Frontiers in Human Neuroscience INTRODUCTION Received: 04 November 2020 Accepted: 17 May 2021 A deficit in executive function is one of the core cognitive deficits in attention-deficit/hyperactivity Published: 18 June 2021 disorder (ADHD) (Willcutt et al., 2005), a condition which can persist from early childhood to Citation: young adulthood (Biederman et al., 2011; Lin and Gau, 2018). In particular, deficits in inhibitory Tsai Y-J, Hsieh S-S, Huang C-J and control in children with ADHD have been considered as an endophenotype (McAuley et al., Hung T-M (2021) Dose-Response 2014). Inhibitory control refers to withholding the attention of an individual in response to task- Effects of Acute Aerobic Exercise irrelevant but prepotent information and stays focused on goal-relevant information (Barkley, Intensity on Inhibitory Control in Children With Attention 1997). Children with ADHD have demonstrated weaker inhibitory control signified by longer Deficit/Hyperactivity Disorder. reaction times (RTs) and lower levels of accuracy during neuropsychological testing, compared with Front. Hum. Neurosci. 15:617596. typically developing children (Mullane et al., 2009). Impaired inhibitory control has been associated doi: 10.3389/fnhum.2021.617596 with failures in several cognitive processes such as attention allocation, stimuli evaluation, as well as Frontiers in Human Neuroscience | www.frontiersin.org 1 June 2021 | Volume 15 | Article 617596 Tsai et al. Exercise Intensity and Inhibitory Control action monitoring (Doehnert et al., 2010; Liotti et al., 2010; there may be a dose-response effect of acute aerobic exercise Kratz et al., 2011). Given that inhibitory control is one intensity on inhibitory control in children with ADHD. of the cornerstones of complex cognitive operations (e.g., The differential effects of low, moderate, and vigorous- cognitive flexibility and planning) (Miyake et al., 2000), and intensity aerobic exercises on inhibitory control may be that deficits in this cognitive domain are one of the neuro- accounted for, at least in part, by fluctuations in cortical arousal. pathologies in children with ADHD (McAuley et al., 2014), Davey (1973) postulates that moderate-intensity aerobic exercise understanding approaches that facilitate inhibitory control may results in an optimal level of cortical arousal, which, in turn, be of significance. facilitates cognitive performance, whereas low- and vigorous- A growing body of evidence has demonstrated a positive intensity exercise may lead to suboptimal and excessive cortical effect of acute aerobic exercise on inhibitory control in children arousal, thereby compromising cognitive performance. This with ADHD (Chang et al., 2012; Pontifex et al., 2013; Chuang inverted-U shape relation has been verified in non-clinical, et al., 2015; Piepmeier et al., 2015). In particular, previous studies typically developed populations (Kamijo et al., 2004a; Chang suggested that moderate-intensity aerobic exercise, defined either and Etnier, 2009; Chang et al., 2011), but remain underexplored as 50–70% of heart rate reserve (HRR) (Chang et al., 2012; in children with ADHD. Hypoarousal has been consistently Chuang et al., 2015; Yu et al., 2020) or 60–75% of maximal reported in children with ADHD (Satterfield et al., 1974; HRR (Pontifex et al., 2013; Piepmeier et al., 2015), facilitates Barry et al., 2003; Rowe et al., 2005). The optimal stimulation inhibitory control in children with ADHD. However, the effect of (OS) model suggested that the state of arousal of the central low (<40% HRR) and vigorous-intensity (>70% HRR) exercises nervous system (CNS) drives subsequent response and behavior on inhibitory control in children with ADHD is still unclear. (Zentall and Zentall, 1983). According to the OS model, Two studies reported that vigorous-intensity aerobic exercise hypoarousal in children with ADHD, probably results from benefits inhibitory control in children with ADHD. Specifically, deviated maturation/dysfunction in the prefrontal cortex (Strauß Gawrilow et al. (2016) found that children with ADHD exhibited et al., 2018; Zhang et al., 2018), is closely related to inattention better inhibitory control following a single bout of vigorous- and hyperactivity (Rapport et al., 2009). Given the modulatory intensity aerobic exercise. Similarly, Silva et al. (2015) found that effect of acute exercise on arousal (Kamijo et al., 2004a; Chang children with ADHD who underwent vigorous-intensity exercise et al., 2011), it is reasonable to postulate that better cognitive workouts demonstrated identical levels of attention as their performance following acute exercise may be mediated by an typically developing peers, who received no exercise intervention. upregulation of cortical arousal. However, findings from these two studies are confounded by To measure cortical arousal, the current study used alpha the use of between-subjects design with no pre-test measures, oscillations from electroencephalography (EEG). Alpha power, in which pre-existing differences between intervention groups or the amplitude of brainwaves between 8 and 13 Hz frequency cannot be assessed. In addition, one study investigating the band, has been shown to be inversely correlated with mental effects of high-intensity interval exercise found a positive effect activity. Studies also show a relationship between reduced alpha on sustained attention, but findings are confounded by unequal power (i.e., EEG desynchrony) and increased vigilance, alertness, durations between the exercise and non-active control condition and attention (see Oken et al., 2006 for a comprehensive (Medina et al., 2010). Another study employing the same exercise review). Furthermore, attenuation of alpha oscillation is inversely mode and cognitive task found no effect of high-intensity interval associated with fMRI blood-oxygen-level dependent (BOLD) exercise on sustained attention, but in this case, the results are cortical response (Laufs et al., 2006) and is closely related to confounded by individual differences in medication use (Mahon another standardized measure of arousal, skin conductance, with et al., 2013). reduced alpha activity relates to increased skin conductance Moreover, although no previous study investigated the (Barry et al., 2005). These data suggest that reduction in alpha differential effects across low, moderate, and vigorous-intensity power is associated with increased cortical arousal, but despite aerobic exercises on inhibitory control in children with ADHD, this relation, alpha oscillation has not been broadly utilized a meta-analysis of individuals without ADHD indicated that in studying the relationship between exercise, arousal, and high- and moderate-intensity exercises, but not light-intensity cognition in children with ADHD. exercise, benefits cognitive function in adults over 50 years old The Ericksen flanker task has been extensively used to (Northey et al., 2018). In contrast, another meta-analysis found measure inhibitory control in children with ADHD (Mullane that the beneficial effect of vigorous-intensity exercise and high- et al., 2009). It involves participants being instructed to identify a intensity interval training
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